Mechanistically, the increase in fluidity with unsaturation is attributed to the presence of cis double bonds that bend the acyl chains of unsaturated FA, resulting in greater interchain distances and, consequently, in the decrease in van der Waals force of intermolecular attraction ( Hulbert and Else, 1999). More specifically, MPH proposes two interacting molecular mechanisms linking membrane FA composition to the rates of metabolism and ageing.įirst, the incorporation of unsaturated FA (i.e., those containing at least one double bond) into biological membranes enhances membrane fluidity ( Jaureguiberry et al., 2014) and the activity of membrane proteins, which may enable higher cellular and organismal metabolic rates ( Hulbert, 2008). The most prominent of these hypotheses is the membrane pacemaker hypothesis (MPH), which proposes that the level of membrane FA unsaturation could act as a pacemaker of metabolism and ageing, thereby determining species-specific life span ( Hulbert and Else, 1999 Hulbert, 2008).
This fact has sparked the development of hypotheses that propose that the membrane FA composition is a key molecular adaptation underpinning the evolution of metabolic rates, ageing, and life span ( Hulbert and Else, 1999 Pamplona et al., 2002 Hulbert, 2010). The fatty acid (FA) composition of biological membranes has a strong influence on many cellular processes ( Grecco et al., 2011). Therefore, in addition to posing significant challenges to MPH, our results imply that fatty acid composition does not pose an evolutionary constraint underpinning life-history trade-offs at the molecular level. Importantly, maximum life span, annual fecundity, and BMR were associated with different fatty acids or fatty acid indices, indicating that longevity, fecundity, and BMR coevolve with different aspects of fatty acid composition.
Our results rather suggest that long life span evolves with long-chain fatty acids irrespective of their degree of unsaturation as life span was positively associated with at least one long-chain fatty acid of each type (i.e., SFA, MUFA, n-6 PUFA, and n-3 PUFA). Moreover, our analysis provided no evidence for the previously reported links between life span and n-3 PUFA/total PUFA or MUFA proportion. While statistically controlling for the confounding effects of body mass and phylogeny, we found no support for long life span evolving with low fatty acid unsaturation and only very weak support for fatty acid unsaturation acting as a pacemaker of BMR. In this study, we tested the coevolution of liver fatty acid composition with maximum life span, annual fecundity, and basal metabolic rate (BMR), using a recently published data set comprising liver fatty acid composition of 106 avian species. Moreover, some empirical studies suggest that an n-3/n-6 PUFA ratio or the fatty acid chain length, rather than the overall unsaturation, could be the key traits coevolving with life span. However, previous comparative studies testing MPH provide mixed evidence regarding the direction of covariation between fatty acid unsaturation and life span or metabolic rate. MPH could, therefore, provide a mechanistic explanation for trade-offs between longevity, fecundity, and metabolic rates, predicting that short-lived species with fast metabolic rates and higher fecundity would have greater levels of membrane unsaturation. MPH proposes that highly unsaturated membranes enhance cellular metabolic processes while being more prone to oxidative damage, thereby increasing the rates of metabolism and ageing. The fatty acid composition of biological membranes has been hypothesised to be a key molecular adaptation associated with the evolution of metabolic rates, ageing, and life span – the basis of the membrane pacemaker hypothesis (MPH).
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